Protein 600 is a Microtubule/endoplasmic Reticulum-associated Protein in CNS Neurons

Overview

Journal J Neurosci

Specialty Neurology

Date 2008 Apr 4

PMID 18385319

Citations 31

Authors

Su Yeon Shim

Jian Wang

Naoyuki Asada

Gernot Neumayer

Hong Chi Tran

Kei-Ichiro Ishiguro

Kamon Sanada

Yoshihiro Nakatani

Minh Dang Nguyen

Affiliations

Soon will be listed here.

Abstract

There is an increasing body of literature pointing to cytoskeletal proteins as spatial organizers and interactors of organelles. In this study, we identified protein 600 (p600) as a novel microtubule-associated protein (MAP) developmentally regulated in neurons. p600 exhibits the unique feature to interact with the endoplasmic reticulum (ER). Silencing of p600 by RNA interference (RNAi) destabilizes neuronal processes in young primary neurons undergoing neurite extension and containing scarce staining of the ER marker Bip. Furthermore, in utero electroporation of p600 RNAi alters neuronal migration, a process that depends on synergistic actions of microtubule dynamics and ER functions. p600-depleted migrating neurons display thin, crooked, and "zigzag" leading process with very few ER membranes. Thus, p600 constitutes the only known MAP to associate with the ER in neurons, and this interaction may impact on multiple cellular processes ranging from neuronal development to neuronal maturation and plasticity.

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References

DeMasi J, Huh K, Nakatani Y, Munger K, Howley P . Bovine papillomavirus E7 transformation function correlates with cellular p600 protein binding. Proc Natl Acad Sci U S A. 2005; 102(32):11486-91. PMC: 1182553. DOI: 10.1073/pnas.0505322102. View

Nguyen M, Shu T, Sanada K, Lariviere R, Tseng H, Park S . A NUDEL-dependent mechanism of neurofilament assembly regulates the integrity of CNS neurons. Nat Cell Biol. 2004; 6(7):595-608. DOI: 10.1038/ncb1139. View

Xie Z, Tsai L . Cdk5 phosphorylation of FAK regulates centrosome-associated miocrotubules and neuronal migration. Cell Cycle. 2004; 3(2):108-10. View

Waterman-Storer C, Salmon E . Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol. 1998; 8(14):798-806. DOI: 10.1016/s0960-9822(98)70321-5. View

Gil P, Dewey E, Friml J, Zhao Y, Snowden K, Putterill J . BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 2001; 15(15):1985-97. PMC: 312751. DOI: 10.1101/gad.905201. View

Nakatani Y, Konishi H, Vassilev A, Kurooka H, Ishiguro K, Sawada J . p600, a unique protein required for membrane morphogenesis and cell survival. Proc Natl Acad Sci U S A. 2005; 102(42):15093-8. PMC: 1247991. DOI: 10.1073/pnas.0507458102. View

Sanada K, Tsai L . G protein betagamma subunits and AGS3 control spindle orientation and asymmetric cell fate of cerebral cortical progenitors. Cell. 2005; 122(1):119-31. DOI: 10.1016/j.cell.2005.05.009. View

Galjart N . CLIPs and CLASPs and cellular dynamics. Nat Rev Mol Cell Biol. 2005; 6(6):487-98. DOI: 10.1038/nrm1664. View

Rakic P . The radial edifice of cortical architecture: from neuronal silhouettes to genetic engineering. Brain Res Rev. 2007; 55(2):204-19. PMC: 2203611. DOI: 10.1016/j.brainresrev.2007.02.010. View

10.

Rinnerthaler G, Geiger B, Small J . Contact formation during fibroblast locomotion: involvement of membrane ruffles and microtubules. J Cell Biol. 1988; 106(3):747-60. PMC: 2115107. DOI: 10.1083/jcb.106.3.747. View

11.

Dent E, Gertler F . Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron. 2003; 40(2):209-27. DOI: 10.1016/s0896-6273(03)00633-0. View

12.

Ghashghaei H, Lai C, Anton E . Neuronal migration in the adult brain: are we there yet?. Nat Rev Neurosci. 2007; 8(2):141-51. DOI: 10.1038/nrn2074. View

13.

Terasaki M, Chen L, Fujiwara K . Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol. 1986; 103(4):1557-68. PMC: 2114338. DOI: 10.1083/jcb.103.4.1557. View

14.

Verkhratsky A . Endoplasmic reticulum calcium signaling in nerve cells. Biol Res. 2005; 37(4):693-9. DOI: 10.4067/s0716-97602004000400027. View

15.

Ezratty E, Partridge M, Gundersen G . Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol. 2005; 7(6):581-90. DOI: 10.1038/ncb1262. View

16.

Hirotsune S, Fleck M, Gambello M, Bix G, Chen A, Clark G . Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet. 1998; 19(4):333-9. DOI: 10.1038/1221. View

17.

Lee M, Tuttle J, REBHUN L, Cleveland D, Frankfurter A . The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton. 1990; 17(2):118-32. DOI: 10.1002/cm.970170207. View

18.

Dreier L, Rapoport T . In vitro formation of the endoplasmic reticulum occurs independently of microtubules by a controlled fusion reaction. J Cell Biol. 2000; 148(5):883-98. PMC: 2174540. DOI: 10.1083/jcb.148.5.883. View

19.

Klopfenstein D, Kappeler F, Hauri H . A novel direct interaction of endoplasmic reticulum with microtubules. EMBO J. 1998; 17(21):6168-77. PMC: 1170943. DOI: 10.1093/emboj/17.21.6168. View

20.

DAILEY M, Bridgman P . Dynamics of the endoplasmic reticulum and other membranous organelles in growth cones of cultured neurons. J Neurosci. 1989; 9(6):1897-909. PMC: 6569719. View